And Hippodamia Variegata (Coleoptera: Coccinellidae) Recorded in the Context of D

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Eur. J. Entomol. 112(3): 453–459, 2015 doi: 10.14411/eje.2015.053 ISSN 1210-5759 (print), 1802-8829 (online)

Demographic parameters of Diuraphis noxia (Hemiptera: Aphididae) and Hippodamia variegata (Coleoptera: Coccinellidae) recorded in the context of D. noxia infesting resistant and susceptible cultivars of wheat

Leila ZANGANEH 1, Hossein MADADI 1, * and Hossein ALLAHYARI 2

1 Department of Plant Protection, Faculty of Agriculture, Bu-Ali Sina University, Hamedan, Iran; e-mails: [email protected]; [email protected] 2 Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran; e-mail: [email protected]

Key words. Hemiptera, Aphididae, Diuraphis noxia, Coleoptera, Coccinellidae, Hippodamia variegata, Russian wheat aphid, life table, host plant resistance

Abstract. The Russian wheat aphid (RWA), Diuraphis noxia (Kurdjumov), is a serious pest of small grains and can cause losses of about 80% in wheat yields. Chemical control is ineffective against this pest so the combined use of host plant resistance and biological control is seen as a possible better means of controlling this pest. In this study, the potential effect of Omid (resistant) and Sardari (susceptible) cultivars of wheat on life table parameters and daily fecundity of RWA and its predator, Hippodamia variegata (Goeze), were determined using the age-stage two-sex life table theory. The results indicate that the rm, R0, λ, T and GRR of RWA were –0.005 ± 0.01 day–1, 0.9 ± 0.24 offspring per individual, 0.99 ± 0.01 day–1, 21.16 ± 1.79 days and 13.34 ± 2.91 offspring on Omid and 0.159 ± 0.01 day–1, 6.9 ± 0.54 offspring per individual, 1.17 ± 0.01 day–1, 12.14 ± 0.26 days and 12.73 ± 1.22 offspring on Sardari. The corresponding values for H. variegata fed on RWA reared on Omid were 0.24 ± 0.01 day–1, 399.35 ± 53.01 eggs, 1.27 ± 0.01 day–1, 24.67 ± 0.28 days and 544.23 ± 75.86 eggs and on Sardari 0.20 ± 0.006 day–1, 221.56 ± 34.68 eggs, 1.23 ± 0.01 day–1, 26.50 ± 0.41 days and 402.72 ± 67.55, respectively. The resistance of wheat cultivars significantly affected life table parameters and mean fecundity of RWA and H. variegata. Our results indicate that combining both host plant resistance and predators in the integrated pest management of RWA could result in a synergistic effect.

Introduction develop resistance to insecticides, which makes their con- The Russian wheat aphid (RWA), Diuraphis noxia trol more difficult (Dogimont et al., 2010). Host plant re- (Kurdjumov) (Hemiptera: Aphididae), is a major pest of sistance is one of the environmentally safe tactics widely small grains, particularly wheat, barley, triticale, rye and used to reduce pest populations (Du Toit, 1987). The use of wild grasses world-wide and a major cause of economic resistant plants may enhance or reduce the ability of natu- losses (Farid et al., 1997; Clark & Messina, 1998; Qing ral enemies to control insect pests (Bottrell et al., 1998; Nian et al., 2009; Jimoh et al., 2013). It prefers to feed Cortesero et al., 2000; Messina & Sorenson, 2001). Re- within the leaf whorl on new leaves (Macedo et al., 2003), sistant plants may affect the efficacy of important natural injecting a toxin that causes leaf discoloration and distor- enemies of D. noxia (Reed et al., 1991) by increasing their tion. Leaf rolling plays an important role in reducing the accessibility to natural enemies (Messina & Sorenson, effectiveness of certain management strategies, by reduc- 2001). Recent evidence indicates that host plant resistance ing contact with insecticides and the efficacy of biologi- and RWA predators or parasitoids can be effectively used cal control agents (Gutsche et al., 2009). When abundant, in combination (e.g. Farid et al., 1997, 1998; Messina & RWA reduces wheat yield directly (Kindler & Hammon, Sorenson, 2001). 1996). Although a poor vector of plant pathogenic viruses, The variegated lady beetle, Hippodamia variegata including barley yellow dwarf virus, barley brome mo- (Goeze) feeds on many insect pests such as aphids, psyl- saic and barley stripe mosaic (Damsteegt et al., 1992), it lids, whiteflies and mealybugs (Franzman, 2002). This spe- nevertheless can reduce the yield of wheat by up to 80% cies is reported as an important natural enemy of at least (Hughes & Maywald, 1990). 12 different species of aphids infesting a diversity of crops It is difficult to manage RWA because it has a short life (Franzmann, 2002; Kontodimas & Stathas, 2005). H. va cycle and an extremely high reproductive rate (Dogimont riegata is part of the natural enemy complex of RWA in et al., 2010). Insecticides are frequently used to suppress Iran and plays a major role in reducing the abundance of RWA populations but in addition to environmental pollu- this aphid. Therefore, understanding the tritrophic ecology tion and risk to non-target beneficial insects, aphids can of this predator helps to better control RWA in different situations.

* Corresponding author. 453 Life table studies are fundamental to population ecol- An excess of aphids was provided to each pair and the number of ogy (Chi & Yang, 2003; Zu et al., 2005). They provide a eggs produced by each pair recorded daily. If one member of a brief description of mortality, survival, development, age pair (male or female) in each replicate died, the experiment was structure and fecundity of a cohort of animals (Chi & Yang, continued until the death of the last individual. All experiments were conducted under constant conditions (25 ± 1°C, 60 ± 5% 2003; Gabre et al., 2005; Zu et al., 2005; Huang & Chi, R.H. and a 16L : 8D photoperiod). 2011). Moreover, life table parameters are one of the best criteria for assessing the effects of different kinds of prey Data analysis on predator survival and fecundity (Golizadeh & Jafari- Raw data were analyzed based on the age-stage, two-sex life Behi, 2012). Tritrophic studies have shown that in many table method (Chi & Liu, 1985; Chi, 1988) in the software pro- cases, the nutritional quality of host plants affect prey and gram TWOSEX-MS Chart (available at http://140.120.197.173/ Ecology/prod02.htm) (National Chung Hsing University, Tai- predator life histories (Bottrell et al., 1998; Wu et al., 2010). chung, Taiwan) and at http://nhsbig.inhs.uiuc.edu/wes/chi.html Therefore, it is necessary to study the life table of preda- (Illinois Natural History Survey, Champaign-Urbana, IL) (Zu et tors fed on prey reared on different host plants. Although al., 2005; Atlihan & Chi, 2008). This method differs from tra- many studies have recorded the life tables of different spe- ditional female-based life table analysis in including preadult cies of lady beetles and aphids, there are few controlled mortality, variation in the developmental rate of adults and the studies on the effect of prey feeding history on the life his- male contribution to the demographic parameters. Moreover, be- tory parameters of H. variegata. Moreover, most studies cause mean duration or “adult age” is generally used to construct have used female age-specific life table to analyse the data the survival curve, this results in errors in population parameters whereas in this study age-stage two-sex life table is used. (Chi & Liu, 1985; Chi, 1988). The age-stage, two-sex life table is widely used in studies on parthenogenic species (He et al., 2013; The main aim of this paper is to study the effect of resistant Hu et al., 2014). and susceptible cultivars of wheat on the life history and The most important life history parameter, i.e., intrinsic rate of demographic parameters of RWA and H. variegata. increase (rm) was calculated using the Euler-Lotka equation (1), ∞ −r ( x +1 ) Material and methods m ∑ l x m x e =1 (1) x=0 Insect and plant rearing where, x is the age of the aphid (days), l is the age-specific sur- Two wheat cultivars, the resistant Omid and susceptible Sardari x vival rate and m is the age-specific fecundity rate. Based on the (Kazemi et al., 2001; Najafi Mirak et al., 2004; Dolati et al., 2004) x age-stage two-sex life table, the values of l and m are calculated were grown in plastic pots in a greenhouse kept at 25 ± 5°C, 55 ± x x as: 10% relative humidity and a 12L : 12D photoperiod (Department k of Plant Protection, Faculty of Agriculture, Bu-Ali Sina Univer- l x=∑ sxj (2) sity, Iran). Russian wheat aphids were collected from different j=1 parts of Hamedan province in western Iran. Wheat plants infested k with D. noxia provided sufficient numbers of RWA for the experi- ∑ sxj f xj ments and the colonies were maintained on two cultivars of wheat j=1 m = (3) for at least three generations. H. variegata were collected from an x k alfalfa field (Hamedan, Amzajerd region, 35°1´N, 48°31´E) and ∑ s xj fed by aphids reared on either the resistant or susceptible cultivar j=1 of wheat for at least three generations before starting the experi- where, k is the number of stages, x = age, j = stage, sxj is the age- ment. stage survival rate (Chi, 1988; Chi & Yang, 2003). In addition, life expectancy (e ), mean fecundity (F) of individ- Life tables of D. noxia and H. variegata xj ual of age x and stage y and other parameters such as net repro- To obtain each RWA cohort, five adults were placed in cylin- ductive rate (R0), finite rate of increase (λ), T (mean generation drical clip cages (30 mm diameter) one of which was clipped to time) and gross reproductive rate (GRR) were also calculated. each of the leaves of a wheat seedling. After 12 h, all but one Because the jackknife method provides incorrect estimates of the individual were removed leaving a single first instar nymph in standard errors for R0 (Jha et al., 2012), bootstrap techniques were each cage. Because, many of the RWA nymphs died prematurely used to estimate uncertainty (Efron & Tibshirani, 1993). Inde- on the resistant cultivar, the number of first instar nymphs reared pendent sample t-tests or non-parametric Mann-Whitney U tests on the resistant and susceptible cultivars was 202 and 100, respectively. Experimental plants were checked daily and nymphal Table 1. Population parameters (± SE) of Diuraphis noxia mortality and developmental time were recorded. After reach- reared on Sadari, a susceptible and Omid, a resistant cultivar of ing the adult stage, reproduction was recorded by removing the wheat. newborn nymphs daily. This procedure continued until the adult Wheat cultivar aphids died. Parameter (Unit) A similar procedure was used for studying the life table param- Sardari Omid –1 eters of H. variegata. Lady beetle adults were reared separately rm (day ) 0.159 ± 0.01 –0.005 ± 0.01 on either D. noxia reared on resistant or susceptible wheat before R0 (offspring) 6.9 ± 0.54 0.9 ± 0.24 the start of the experiment. Then, 107 and 113 newly laid eggs λ (day –1) 1.172 ± 0.01 0.995 ± 0.01 were collected from H. variegata fed on aphids of resistant and T (day) 12.14 ± 0.26 21.16 ± 1.79 susceptible wheat seedlings, respectively. After hatching, the lar- GRR (offspring) 12.73 ± 1.22 13.34 ± 2.91 vae were provided with either mixed stages of Omid- or Sardari- reared aphids and as soon as they became adult they were sexed rm – intrinsic rate of increase; R0 – net reproductive rate; λ – finite and paired randomly in ventilated Petri dishes (9-cm diameter). rate of increase; T – mean generation time; GRR – gross reproductive rate. 454 Fig. 1. Trends in time of the age-stage survival rate (lx), age- Fig. 2. Trends in the age-stage survival rate (lx), age-specific fe- specific fecundity (mx) and maternity (lx·mx) rate of Diuraphis cundity (mx) and maternity (lx·mx) rate of Diuraphis noxia reared noxia reared on Omid, a resistant cultivar of wheat. on Sardari, a susceptible cultivar of wheat. were used to compare life history parameters whenever normality dant stage followed by first instar nymphs. As the differ- assumptions were not met. In all tests, α was 0.05. ent stages of D. noxia have different developmental rates Results (Fig. 3) there are overlaps in the survival rate curves. This point is ignored in analyses using female-based life tables. Life history parameters of RWA In addition, Fig. 3 indicates that the survival rates of all life Demographic parameters of RWA reared on resistant and stages were highest on the susceptible cultivar. Reproduc- susceptible cultivars of wheat are given in Table 1. The dif- tive value, defined as the expected relative contribution of ferences between the rm, R0, λ and T values for RWA reared an individual to future population numbers, maximally oc- on Omid and Sardari cultivars of wheat were significant curred at an age of 11 days on the resistant and 7 days on (Mann-Whitney test, U Statistic = 0.000, P-value < 0.001) the susceptible cultivar. but not those for GRR (Mann-Whitney test, U Statistic = Population parameters of H. variegata 491620.00, P-value = 0.516). A decreasing trend in the sur- The initial number of lady beetle eggs used in the life vival rate of RWA was recorded during the developmental table study were 107 and 113 for those reared on aphids period on both cultivars of wheat, but higher mortalities collected from susceptible and resistant cultivars of wheat, were recorded on the resistant than on the susceptible cul- respectively, of which 90 and 79 reached the adult stage tivar, especially during the early stages of development (84% and 69% survival rates, respectively). Life history (Figs 1 and 2). The age-specific fecundity (m ) indicates x parameters of H. variegata reared on aphids collected from that the number of offspring produced by an individual the resistant and susceptible cultivars of wheat are present- RWA of age x on the resistant cultivar reaches its maxi- ed in Table 3. Values of r (Mann-Whitney test, U Statistic mum value (1.5) at the end of the reproductive period (day m = 0.00, P-value < 0.001), λ (Mann-Whitney test, U Statistic 36), while on the susceptible cultivar the peak (1.024) was = 0.00, P-value < 0.001), R (Mann-Whitney test, U Statis- recorded three days after the start of reproduction. Because 0 tic = 2682.0, P-value < 0.001), T (Mann-Whitney test, U of the low survival rate of RWA on the resistant cultivar Statistic = 135.5, P-value < 0.001) and GRR (Mann-Whit- the net age-specific maternity, [i.e. the weighted average ney test, U Statistic = 81474.00, P-value < 0.001) differed production of offspring by females aged x each day (Carey, for ladybirds reared on the resistant and susceptible culti- 1993)] was very low irrespective of the oscillations in the vars of wheat. The trends in age-specific survival curves age-specific fecundity. However, this parameter followed (l ), age-specific fecundity (m ) and age-specific maternity the same trend as m recorded on the susceptible cultivar. x x x (l ·m ) of H. variegata reared on aphids collected from the The female mean fecundity was 7.24 ± 1.38 and 8.02 ± x x resistant and susceptible cultivars of wheat are illustrated 0.53 on the resistant and susceptible cultivars, respectively. in Fig. 4. These figures indicate that H. variegata reared Stable age distribution of RWA Table 3. Population parameters (mean ± SE) of Hippodamia Table 2 shows the stable age distribution (percentage). variegata fed on Diuraphis noxia reared on Sardari, a susceptible It reveals that on both cultivars adults are the most abun- and Omid, a resistant cultivar of wheat. Symbols in Table1.

Table 2. Percentage of individuals in each of the developmen- Parameter Omid Sardari tal stages in populations of Diuraphis noxia at stable age distribu- –1 rm (d ) 0.24 ± 0.01 0.20 ± 0.01 tion on Omid and Sardari cultivars of wheat. R0 (offspring) 399.35 ± 53.01 221.56 ± 34.68 Wheat cultivar 1st instar 2nd instar 3rd instar 4th instar Adult λ (d–1) 1.27 ± 0.01 1.23 ± 0.01 Omid 29.98 14. 17 14.32 8.86 32.93 T (day) 24.67 ± 0.28 26.50 ± 0.41 Sardari 27.30 18.22 13.47 8.36 32.46 GRR (offspring) 544.23 ± 75.86 402.72 ± 67.55

455 Fig. 3. Survival rate of each age-stage of D. noxia reared on the resistant Omid (left) and susceptible Sardari (right) cultivars of wheat. on aphids collected from the susceptible cultivar of wheat stable age distribution of H. variegata in both cases are started laying eggs on day 17 and ceased on day 85 (68 similar, with more than half of the lady beetle population days), while those reared on aphids collected from the re- made up of eggs and third instar larvae the least abundant sistant cultivar of wheat started laying eggs on day 16 and of the larval stages. ceased on day 63 (47 days). However, the oscillations in Discussion the age-specific fecundity recorded for H. variegata fed RWA reared on the resistant cultivar were greater than for This tritrophic study confirmed that the nutritional qual- those fed RWA reared on the susceptible cultivar (Fig. 4). ity of a host plant affects both the herbivore that feeds on it Plant resistance affected maximum daily and maximum and its natural enemy. The lower values of life table param- total fecundity of H. variegata with 142 and 125 eggs, and eters (rm, R0 and λ) recorded for RWA reared on the resist- 1716 and 1480 eggs for lady beetles fed D. noxia reared ant cultivar of wheat demonstrate the effectiveness of plant on the resistant and susceptible cultivars of wheat, respec- resistance against RWA. When reared on the resistant cul- tively. Maximum reproductive values of H. variegata fed tivar the intrinsic rate of increase (rm) of RWA was negative D. noxia reared on the resistant and susceptible cultivars of (i.e. the population decreased). This might be due to higher wheat were 101.63 and 79.29, which were recorded when immature mortality or reduced fecundity. The age-stage they were 18 and 21 days old, respectively. Survival curves survival rate (lx) curve indicates that more than half of the of H. variegata recorded over the complete developmental nymphs died before reaching the second instar when reared period when fed aphids reared on both cultivars of wheat on the resistant cultivar. In addition, the net reproductive were similar (Fig. 5). The overlapping curves reflect the rate (R0) and the finite rate of increase (λ) ofD. noxia were different developmental rates of the different stages. similarly dependent on the cultivar of wheat they were reared on. Furthermore, on the resistant wheat cultivar the Stable age distribution of H. variegata developmental period and mean generation time (T) of D. The stable age distributions of H. variegata fed RWA noxia were longer. This effect has consequences in terms reared on both cultivars of wheat are shown in Table 4. The of the temporal availability of aphids for natural enemies.

Fig. 4. Trends in the age specific survival (lx), age-specific fecundity (mx) and maternity (lx·mx) of Hippodamia variegata fed on Rus- sian wheat aphids reared on Omid (R, left) and Sardari (S, right) cultivars of wheat.

456 Fig. 5. Survival rate of each age-stage of Hippodamia variegata fed on Russian wheat aphids reared on Omid (R, left) and Sardari (S, right) cultivars of wheat.

As developmental time increases, the chances of natural tabolites of the resistant cultivar might have had adverse enemies finding and killing an aphid increases. effects on RWA but when metabolized by the aphid have a A study of the resistance of five cultivars of wheat: Ala- positive effect on the reproduction and survival of H. var moot, Alvand, Zarrin, Sabalan and Sardari, to RWA under iegata relative to that recorded when fed the aphid reared field conditions in Tabriz, northwest of Iran, indicates that on a susceptible cultivar that lacks these metabolites (Bark- the greatest and the lowest numbers of progeny produced hordar et al., 2013). In addition, it is possible these differ- / female over the first 10 and 15 days of reproduction, re- ences are a consequence of differences for H. variegata in spectively, are 34.94 ± 5.91 and 48.56 ± 7.66 on Sardari the digestibility of RWA reared on resistant and susceptible and 24.83 ± 9.36 and 36.67 ± 13.67 on Alvand (Kazemi et cultivars (Barkhordar et al., 2013). al., 2001). Moreover, the highest rm values recorded within The life history of H. variegata reared at different tem- 10 and 15 days were 0.268 ± 0.02 day–1 and 0.264 ± 0.02 peratures and on different diets is well studied. Differences day–1, respectively for individuals reared on Sardari and the are reported in the demographic parameters of H. varie lowest, 0.217 ± 0.03 day–1 and 0.223 ± 0.03 day–1 on Al- gata fed on different species of aphids. El Hag & Zaitoon vand. Effects of different temperatures and different barley (1996) compare four species of coccinellids in terms of plant growth stages on life table parameters of RWA are their biological parameters and report an rm value of 0.082 reported by Ma & Bechinski (2009) who record the highest day–1 for H. variegata. Mollashahi et al. (2004) studied intrinsic rate of increase as 0.288 day–1 at 25.08°C on stage population growth parameters of H. variegata fed on Aphis 12 (Zadoks scale). Veisi et al. (2012) record total fecundi- gossypii Glover and report that the intrinsic rate of increase ties of 61.75 ± 7.93 and 24.00 ± 0.81, and mean offspring (rm) and net reproductive rate (R0) of this predator are 0.254 produced per female per day of 2.51 ± 0.43 and 1.40 ± 0.19 day–1 and 387.9 eggs, respectively. Lanzoni et al. (2004) on the cultivars Yavarus and Omid, respectively. Overall, report an intrinsic rate of increase of 0.114 day–1 for H. they conclude that Yavarus is susceptible and Omid resist- variegata, which is higher than that of Harmonia axyridis ant to RWA. (Pallas) and Adalia bipunctata (L.) fed on Myzus persicae

The most striking finding of our study is that plant qual- (Sulzer). Farhadi et al. (2011) report an rm value of 0.203 ± ity positively affects the life history parameters of H. var 0.005 day–1 for H. variegata fed bean aphids, Aphis fabae iegata. Based on the rm and other demographic parameters Scopoli, which is similar to the value recorded in this study of H. variegata, the resistance of wheat to D. noxia did for H. variegata fed on RWA reared on the susceptible cul- not negatively affect the growth, survival and fecundity, tivar of wheat. In addition, parameters other than R0 have and improved the population growth of H. variegata. That similar values. The rm of H. variegata fed on A. gossypii is is, H. variegata grew faster and laid more eggs when feed 0.179 ± 0.005 day–1 (Bigdelou, 2012). on RWA reared on a resistant than on an aphid-susceptible Our results indicate that not only the type of prey but also cultivar of wheat. This dual effect of host plant resistance the quality of the host plant of the prey can have substantial may be of chemical origin. Natural secondary plant me- indirect effects on the life table parameters and effectiveness of ladybirds. This is also reported for other predator- prey systems (Ofuya, 1995; Wu et al., 2010). Farid et al. Table 4. Stable age distributions (%) of populations of Hippo damia variegata fed on aphids reared on Sadari, a susceptible and (1997) report that the percentage mortality of Scymnus Omid, a resistant cultivar of wheat. frontalis (Fabricius, 1787) (Coleoptera: Coccinellidae) lar- Cultivar Egg L L L L Pupae Female Male vae is higher on susceptible than on RWA-resistant plants 1 2 3 4 and attribute this to the greater incidence of entrapment of Omid 53.48 21.55 7.78 5.30 6.53 2.95 1.24 1.18 D. noxia by curled leaves of susceptible cultivars of wheat. Sardari 50.69 20.90 8.08 6.42 7.04 3.47 1.70 1.69

457 Cultivar resistance did not affect the weight of the larvae, of wheat. It is probable that application of this predator on prepupae, pupae and adults or the total developmental time a resistant cultivar might lead to a greater synergistic effect of S. frontalis. Different results are reported by Brewer et in RWA population. However, it is unclear if this effect is al. (1998) who show that use of barley resistant to RWA chemically mediated and if so, what the biochemical basis results in a decrease in the abundance of Diaeretiella rapae for it is. (Mc Intosh) and Aphelinus albipodus Hayat & Fatima as AcknowledgEments. We are grateful to M. Sameni and T. aphid abundance decreases, even though parasitism rates Behnazar for their cooperation. Special thanks to F. Shirzadi for were expected to be approximately equal on resistant and editing an early draft of the manuscript. This study was funded susceptible barley. Farid et al. (1998) report that although by the Faculty of Agriculture, Bu-Ali Sina University, Hamedan, the rate of population increase of D. noxia is lower on a Iran and formed a part of the M.Sc. thesis of the first author. resistant cultivar of wheat over a period of three generations, plant resistance did not have a negative effect on References percentage emergence, sex ratio, adult longevity, or head Atlihan R. & Chi H. 2008: Temperature-dependent development width of D. rapae. Furthermore, when parasitoids emerge and demography of Scymnus subvillosus (Coleoptera: Coc- from aphids reared on resistant cultivars the longevity of cinellidae) reared on Hyalopterus pruni (Homoptera: Aphidi- females is greater. Thus, host plant resistance can affect dae). — J. Econ. Entomol. 101: 325–333. both growth and development of D. rapae. The abundance Barkhordar B., Khalghani J., Salehi Jouzani G., Nouri Gan- of D. noxia on resistant barley lines is lower than on more balani G., Shojai M., Boustani M.T., Karimi E., Soheilivand S. & Hosseini B. 2013: Impact of host plant resistance on the susceptible lines (Brewer et al., 1998). In addition, the tritrophic interactions between wheat genotypes, Schizaphis abundance of the parasitoids D. rapae, A. albipodus and graminum (Homoptera: Aphididae), and Coccinella septem Aphelinus asychis Walker, 1839 on resistant and suscepti- punctata (Coleoptera: Coccinellidae) using molecular meth- ble barley lines is similar (Brewer et al., 1999). They also ods. — Environ. Entomol. 42: 1118–1122. conclude that in this system, the use of plant resistance and Bigdelou B. 2012: Life Table and Predation Capacity of Hippo- natural enemies are compatible strategies. damia variegata (Col.: Coccinellidae) Feeding on Aphis gos- The larvae of the lacewing Chrysoperla plorabunda sypii (Hem.: Aphididae). MSc. Thesis, University of Tehran, (Fitch) cause a greater proportional reduction in the abun- 97 pp. dance of RWA on resistant than on near isogenic suscep- Bosque-Perez N.A., Johnson J.B. Schotzko D.J. & Unger L. 2002: Species diversity, abundance, and phenology of aphid tible lines of wheat, which indicates that lacewings are natural enemies on spring wheats resistant and susceptible to more effective on resistant plants (Messina & Sorenson, Russian wheat aphid. — BioControl 47: 667–684. 2001). The smaller aphid populations or smaller size of Bottrell D.G., Barbosa P. & Gould F. 1998: Manipulating natu- individual prey on resistant cultivars may in this case be ral enemies by plant variety selection and modification: a real- the cause of the increase in predator effectiveness (Messina istic strategy? — Annu. Rev. Entomol. 43: 347–367. & Sorenson, 2001). Only the larvae of lacewings prey on Brewer M.J., Struttmann J.M. & Mornhinweg D.W. 1998: Ap aphids and therefore they are less exposed to the defensive helinus albipodus (Hymenoptera: Aphelinidae) and Diaeretiel chemicals of resistant plants. In spring wheat fields in Mos- la rapae (Hymenoptera: Braconidae) parasitism on Diuraphis cow, Idaho there is no interaction between plant resistance noxia (Homoptera: Aphididae) infesting barley plants differing in plant resistance to aphids. — Biol. Contr. 11: 255–261. and the population densities of predators and parasitoids Brewer M.J., Dolores W.M. & Huzurbazar S. 1999: Compati (Bosque-Perez et al., 2002). Thus, D. noxia resistant lines bility of insect management strategies: Diuraphis noxia abun- do not have any adverse effects on the natural enemies dance on susceptible and resistant barley in the presence of (parasitoids and predators) of D. noxia. However, other parasitoids. — BioControl 43: 479–491. studies have demonstrated negative effects of Bt-crops and Carey J.R. 1993: Applied Demography for Biologists. Oxford resistant varieties on parasitoid and predator biology and University Press, New York, 206 pp. fecundity (Schuler et al., 1999). Chi H. 1988: Life table analysis incorporating both sexes and The current study highlights the effect of plant resistance variable developmental rates among individuals. — Environ. on the 3rd trophic level. If the positive effect of resistant Entomol. 17: 26–34. Chi H. & Liu H. 1985: Two new methods for the study of insect cultivars on H. variegata is shown to occur in the field then population ecology. — Bull. Inst. Zool. Acad. Sin. (Taipei) 24: the release of a fixed number of H. variegata should de- 225–240. crease prey abundance even in the lower populations re- Chi H. & Yang T.C. 2003: Two-sex life table and predation rate of corded on resistant cultivars (Messina & Sorenson, 2001). Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed These results increase our understanding of the effects of on Myzus persicae (Sulzer) (Homoptera: Aphididae). — Envi host resistance on natural enemy biology and if relevant to ron. Entomol. 32: 327–333. field conditions, the possibility of important interactions in Clark T.L. & Messina F.J. 1998: Foraging behavior of lacewing IPM programs. A biocontrol agent, especially a parasitoid larvae (Neuroptera: Chrysopidae) on plants with divergent would be more effective if it had a higher r than its host. architectures. — J. Insect Behav. 11: 303–317. m Cortesero A.M., Stapel J.O. & Lewis W.J. 2000: Underestanding In the present study, the ladybird beetles reared on two dif- and manipulating plant attributes to enhance biological control. ferent types of prey had higher rates of increase than RWA, — Biol. Contr. 17: 35–49. which indicates that H. variegata is a suitable candidate Damsteegt V.D., Gildow F.E., Hewings A.D. & Carroll T.W. for release against RWA, especially on resistant cultivars 1992: Clone of the Russian wheat aphid (Diuraphis noxia) as a

458 vector of barley yellow dwarf, barley stripe mosaic, and brome Jimoh M.A., Kaehler S. & Botha C.E.J. 2013: Increased feed-

mosaic viruses. — Plant Dis. 76: 1155–1160. ing damage under elevated CO2: the case of the Russian wheat Dogimont C., Bendahmane A., Chovelon V. & Boissot N. 2010: aphid. — Sth. Afr. J. Bot. 84: 30–37. Host plant resistance to aphids in cultivated crops: Genetic and Kazemi M.H., Mashhadi Jafarloo M., Talebi Chaichi P. & Shak- molecular bases, and interactions with aphid populations. — iba M.R. 2001: Biological responses of Russian Wheat Aphid, C. R. Biol. 333: 566–573. Diuraphis noxia (Kurdjumov, 1913) to certain wheat cultivars Dolati L., Ghareyazie B., Moharramipour S. & Noori-Daloii at emergence stage. — J. Agric. Sci. Technol. 3: 249–255. M.R. 2004: Evidence for regional diversity and host adaptation Kindler S.D. & Hammon R.W. 1996: Comparison of host suit- in Iranian populations of the Russian wheat aphid. — Entomol. ability of western wheat aphid with the Russian wheat aphid. Exp. Appl. 114: 171–180. — J. Econ. Entomol. 89: 1621–1630. Du Toit F. 1987: Resistance in wheat (Triticum aestivum) to Diu Kontodimas D.C. & Stathas G.J. 2005: Phenology, fecundity raphis noxia (Hemiptera: Aphididae). — Cereal Res. Commun. and life table parameters of the predator Hippodamia variegata 15: 175–179. reared on Dysaphis crataegi. — BioControl 50: 223–233. Efron B. & Tibshirani R.J. 1993: An Introduction to the Boot Lanzoni A., Accinelli G., Bazzocchi G.G. & Burgio G. 2004: strap. Chapman and Hall, New York, 436 pp. Biological traits and life table of the exotic Harmonia axyridis El Hag E.T.A. & Zaitoon A.A. 1996: Biological parameters for compared with Hippodamia variegata, and Adalia bipunctata four coccinellid species in central Saudi Arabia. — Biol. Contr. (Col., Coccinellidae). — J. Appl. Entomol. 128: 298–306. 7: 316–319. Ma Z. & Bechinski E.J. 2009: Life tables and demographic sta- Farhadi R., Allahyari H. & Chi H. 2011: Life table and preda- tistics of Russian wheat aphid (Hemiptera: Aphididae) reared tion capacity of Hippodamia variegata (Coleoptera: Coccinel- at different temperatures and on different host plant growth lidae) feeding on Aphis fabae (Hemiptera: Aphididae). — Biol. stages. — Eur. J. Entomol. 106: 205–210. Contr. 59: 83–89. Macedo T.B., Higley L.G. & Ni X. 2003: Light activation of Rus- Farid A., Johnson J.B. & Quisenberry S.S. 1997: Compatibility sian wheat aphid-elicited physiological responses in suscepti- of a coccinellid predator with a Russian wheat aphid resistant ble wheat. — J. Econ. Entomol. 96: 194–201. wheat. — J. Kans. Entomol. Soc. 70: 114–119. Messina F.J. & Sorenson S.M. 2001: Effectiveness of lacewing Farid A., Johnson J.B. Shafii B. & Quisenberry S.S. 1998: Tri- larvae in reducing Russian wheat aphid populations on suscep- trophic studies of Russian wheat aphid, a parasitoid, and re- tible and resistant wheat. — Biol. Contr. 21: 19–26. sistant and susceptible wheat over three parasitoid generations. Mollashahi M., Sahragard A. & Hossaini R. 2004: Determina- — Biol. Contr. 12: 1–6. tion of life table parameters of lady beetle, Hippodamia var Franzmann B.A. 2002: Hippodamia variegata (Goeze) (Coleo iegata (Col: Coccinellidae) under laboratory conditions. — J. ptera: Coccinellidae), a predacious ladybird new in Australia. Agric. Sci. 1: 47–60 [in Persian, English abstr.]. — Aust. J. Entomol. 41: 375–377. Najafi Mirak T., Zali A., Hosseinzadeh A., Saidi A., Rasoulian Gabre R.M., Adham F.K. & Chi H. 2005: Life table of Chrys G. & Zeinali H. 2004: Inheritance and allelism of resistance to omya megacephala (Fabricius) (Diptera: Calliphoridae). — Russian wheat aphid, Diuraphis noxia (Mordvilko) in Iranian Acta Oecol. 27: 179–183. wheat cultivars. — Int. J. Agric. Biol. 6: 525–528. Golizadeh A. & Jafari-Behi V. 2012: Biological traits and life Ofuya T.I. 1995: Colonization and control of Aphis craccivora table parameters of variegated lady beetle, Hippodamia var Koch (Homoptera: Aphididae) by coccinellid predators in iegata (Coleoptera: Coccinellidae) on three aphid species. — some resistant and susceptible cowpea in Nigeria. — J. Crop Appl. Entomol. Zool. 47: 199–205. Prot. 14: 47–50. Gutsche A.R., Heng-Moss T.M., Higley L.G., Sarath G. & Qing Nian C., Xiao M.M., Zhao X., Zhong Y.C. & Yang X.Q. Mornhinweg D.W. 2009: Physiological responses of resistant 2009: Effects of host plant resistance on insect pests and its and susceptible barley, Hordeum vulgare to the Russian wheat parasitoid: A case study of wheat-aphid-parasitoid system. — aphid, Diuraphis noxia (Kurdjumov, 1913). — Arthrop. Plant Biol. Contr. 49: 134–138. Interact. 3: 233–240. Reed D.K., Webster J.A., Jones B.G. & Burd J.D. 1991: Tri- He J., Gao H., Cao Z., Monika W. & Zhao H. 2013: Life table trophic relationships of Russian wheat aphid (Homoptera: analysis of the performance of aphid Sitobion avenae (Homo Aphididae), a hymenopterous parasitoid (Diaeretiella rapae ptera: Aphididae) nymphs exposed to a static magnetic field. McIntosh), and resistant and susceptible small grains. — Biol. — Arch. Biol. Sci. (Belgrade) 65: 1415–1422. Contr. 1: 35–41. Hu Z., Zhao H. & Thieme T. 2014: Comparison of the potential Schuler T.H., Poppy G.M., Kerry B.R. & Denholm I. 1999: Po- rate of population increase of brown and green color morphs tential side effects of insect-resistant transgenic plants on ar- of Sitobion avenae (Homoptera: Aphididae) on barley infected thropod natural enemies. — Trends Biotechnol. 17: 210– 216. and uninfected with Barley yellow dwarf virus. — Insect Sci. Veisi R., Safavi S.A. & Karimpour Y. 2012: Duration of life stag- 21: 326–333. es and fecundity of Diuraphis noxia (Hemiptera: Aphididae) Huang Y.B. & Chi H. 2011: Age-stage, two sex life tables of Bac on six wheat cultivars. — J. Crop Prot. 3: 181–187. trocera cucurbitae (Coquillett) (Diptera: Tephritidae) with a Wu X., Zhou X. & Pang B. 2010: Influence of five host plants discussion on the problem of applying female age-specific life of Aphis gossypii Glover on some population parameters tables to insect populations. — Insect Sci. 19: 263–273. of Hippodamia variegata (Goeze). — J. Pest Sci. 83: 77–83. Hughes R.D. & Maywald G.F. 1990: Forecasting the favora- Zu J.Z., Chi H. & Chen B.H. 2005: Life table and predation of bleness of the Australian environment for the Russian wheat Lemnia biplagiata (Coleoptera: Coccinellidae) fed on Aphis aphid, Diuraphis noxia and its potential impact on Australian gossypii (Homoptera: Aphididae) with a proof on relationship wheat yields. — Bull. Entomol. Res. 80: 165–175. among gross reproduction rate, net reproduction rate, and prea- Jha R.K., Chi H. & Tang L.C. 2012: Life table of Helicoverpa dult survivorship. — Ann. Entomol. Soc. Am. 98: 475–482. armigera (Hubner) (Lepidoptera: Noctuidae) with a discussion on Jackknife vs. Bootstrap techniques and variations on the Received June 16, 2014; revised and accepted February 12, 2015 Prepublished online March 20, 2015 Euler-Lotka equation. — Form. Entomol. 32: 355–375.

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